Tuning and timing in mammalian type i hair cells and calyceal synapses

Journal of Neuroscience

Volumn 33, Issue 8, 2013, Pages 3706-3724

  Songer, Jocelyn E ^a,b   Eatock, Ruth Anne ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; AUDITORY THRESHOLD; CELL MEMBRANE RESISTANCE; CONTROLLED STUDY; ELECTRIC CAPACITANCE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HAIR CELL; ION CURRENT; MALE; MECHANICAL STIMULATION; NERVE CELL MEMBRANE CONDUCTANCE; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; SACCULUS; SIGNAL TRANSDUCTION; SPIKE WAVE; SYNAPSE; SYNAPTIC TRANSMISSION; TEMPERATURE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CELL MEMBRANE; FEMALE; HAIR CELLS, VESTIBULAR; MALE; RATS; RATS, LONG-EVANS; REACTION TIME; SACCULE AND UTRICLE; SYNAPSES;

EID: 84874197762     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4067-12.2013     Document Type: Article

References (72)

1. Armand M, Minor LB (2001) Relationship between time and frequency domain analyses of angular head movements in the squirrel monkey. J Comput Neurosci 11:217-239. CrossRef Medline
2. Art JJ, Fettiplace R (1987) Variation of membrane properties in hair cells isolated from the turtle cochlea. J Physiol 385:207-242. Medline
3. Baird RA, Desmadryl G, Fernández C, Goldberg JM (1988) The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60:182-203. Medline
4. Barry PH (1994) JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. J Neurosci Methods 51:107-116. Medline
5. Beurg M, Nam JH, Chen Q, Fettiplace R (2010) Calcium balance and mechanotransduction in rat cochlear hair cells. J Neurophysiol 104:18-34. CrossRef Medline
6. Bonsacquet J, Brugeaud A, Compan V, Desmadryl G, Chabbert C (2006) AMPA type glutamate receptor mediates neurotransmission at turtle vestibular calyx synapse. J Physiol 576:63-71. CrossRef Medline
7. Catacuzzeno L, Fioretti B, Perin P, Franciolini F (2004) Spontaneous lowfrequency voltage oscillations in frog saccular hair cells. J Physiol 561: 685-701. CrossRef Medline
8. Cherif S, Cullen KE, Galiana HL (2008) An improved method for the estimation of firing rate dynamics using an optimal digital filter. J Neurosci Methods 173:165-181. Medline
9. Contini D, Zampini V, Tavazzani E, Magistretti J, Russo G, Prigioni I, Masetto S (2012) Intercellular K accumulation depolarizes type I vestibular hair and their associated afferent nerve calyx. Neuroscience 227: 232-246. CrossRef Medline
10. Corey DP, Hudspeth AJ (1980) Mechanical stimulation and micromanipulation with piezoelectric bimorph elements. J Neurosci Methods 3:183-202. Medline
11. Correia MJ, Lang DG (1990) An electrophysiological comparison of solitary type I and type II vestibular hair cells. Neurosci Lett 116:106-111. CrossRef Medline
12. Correia MJ, Ricci AJ, Rennie KJ (1996) Filtering properties of vestibular hair cells: An update. Ann NY Acad Sci 781:138-149. CrossRef Medline
13. Crawford AC, Fettiplace R (1981) An electrical tuning mechanism in turtle cochlear hair cells. J Physiol 312:377-412. Medline
14. Curthoys IS (1983) The development of function of primary vestibular neurons. In: Development of auditory and vestibular systems (Romand R, ed), pp 425-461. New York: Academic.
15. Curthoys IS, Vulovic V (2011) Vestibular primary afferent responses to sound and vibration in the guinea pig. Exp Brain Res 210:347-352. CrossRef Medline
16. Dulon D, Safieddine S, Jones SM, Petit C (2009) Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J Neurosci 29:10474-10487. CrossRef Medline
17. Eatock RA (2000) Adaptation in hair cells. Annu Rev Neurosci 23:285-314. CrossRef Medline
18. Eatock RA, Songer JE (2011) Vestibular hair cells and afferents: two channels for head motion signals. Annu Rev Neurosci 34:501-534. CrossRef Medline
19. Eatock RA, Weiss TF, Otto KL (1991) Dependence of discharge rate on sound pressure level in cochlear nerve fibers of the alligator lizard: implications for cochlear mechanisms. J Neurophysiol 65:1580-1597. Medline
20. Fernández C, Goldberg JM (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J Neurophysiol 39:996-1008. Medline
21. Fettiplace R, Hackney CM (2006) The sensory and motor roles of auditory hair cells. Nat Rev Neurosci 7:19-29. CrossRef Medline
22. Géléoc GS, Holt JR (2003) Developmental acquisition of sensory transduction in hair cells of the mouse inner ear. Nat Neurosci 6:1019-1020. CrossRef Medline
23. Géléoc GS, Risner JR, Holt JR (2004) Developmental acquisition of voltagedependent conductances and sensory signaling in hair cells of the embryonic mouse inner ear. J Neurosci 24:11148-11159. CrossRef Medline
24. Ginzberg RD (1984) Freeze-fracture morphology of the vestibular hiar cellprimary afferent synapse in the chick. J Neurocytol 13:393- 405. CrossRef Medline
25. Goldberg JM (1991) The vestibular end organs: morphological and physiological diversity of afferents. Curr Opin Neurobiol 1:229-235. CrossRef Medline
26. Goldberg JM (1996) A theoretical analysis of intercellular communication between the vestibular type I hair cell and its calyx ending. J Neurophysiol 76:1942-1957.Medline
27. Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130:277-297. CrossRef Medline
28. Goldberg JM, Fernández C (1977) Conduction times and background discharge of vestibular afferents. Brain Res 122:545-550. CrossRef Medline
29. Goldberg JM, Fernández C, Smith CE (1982) Responses of vestibular-nerve afferents in the squirrel monkey to externally applied galvanic currents. Brain Res 252:156-160. CrossRef Medline
30. Goldberg JM, Desmadryl G, Baird RA, Fernández C (1990a) The vestibular nerve of the chinchilla. V. Relation between afferent discharge properties and peripheral innervation patterns in the utricular macula. J Neurophysiol 63:791-804. Medline
31. Goldberg JM, Desmadryl G, Baird RA, Fernández C (1990b) The vestibular nerve of the chinchilla. IV. Discharge properties of utricular afferents. J Neurophysiol 63:781-790. Medline
32. Goutman JD, Glowatzki E (2007) Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc Natl Acad Sci U S A 104:16341-16346. CrossRef Medline
33. Grant L, Yi E, Glowatzki E (2010) Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse. J Neurosci 30:4210-4220. CrossRef Medline
34. Gulley RL, Bagger-Sjöbäck D (1979) Freeze-fracture studies on the synapse between the type I hair cell an the calyceal terminal in the guinea-pig vestibular system. J Neurocytol 8:591-603. CrossRef Medline
35. Holt JC, Chatlani S, Lysakowski A, Goldberg JM (2007) Quantal and nonquantal transmission in calyx-bearing fibers of the turtle posterior crista. J Neurophysiol 98:1083-1101. CrossRef Medline
36. Hudspeth AJ, Lewis RS (1988) A model for electrical resonance and frequency tuning in saccular hair cells of the bull-frog, Rana catesbeiana. J Physiol 400:275-297. Medline
37. Hullar TE, Della Santina CC, Hirvonen T, Lasker DM, Carey JP, Minor LB (2005) Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93:2777-2786. CrossRef Medline
38. Hurley KM, Gaboyard S, Zhong M, Price SD, Wooltorton JR, Lysakowski A, Eatock RA (2006) M-like K currents in type I hair cells and calyx afferent endings of the developing rat utricle. J Neurosci 26:10253-10269. CrossRef Medline
39. Huterer M, Cullen KE (2002) Vestibuloocular reflex dynamics during highfrequency and high-acceleration rotations of the head on body in rhesus monkey. J Neurophysiol 88:13-28. Medline
40. Iwasaki S, Chihara Y, Komuta Y, Ito K, Sahara Y (2008) Low-voltageactivated potassium channels underlie the regulation of intrinsic firing properties of rat vestibular ganglion cells. J Neurophysiol 100:2192-2204. CrossRef Medline
41. Kalluri R, Xue J, Eatock RA (2010) Ion channels set spike timing regularity of mammalian vestibular afferent neurons. J Neurophysiol 104:2034-2051. CrossRef Medline
42. Kennedy HJ (2012) New developments in understanding the mechanisms and function of spontaneous electrical activity in the developing mammalian auditory system. J Assoc Res Otolaryngol 13:437-445. CrossRef Medline
43. Lasker DM, Han GC, Park HJ, Minor LB (2008) Rotational responses of vestibular-nerve afferents innervating the semicircular canals in the C57BL/6 mouse. J Assoc Res Otolaryngol 9:334-348. CrossRef Medline
44. Li A, Xue J, Peterson EH (2008) Architecture of the mouse utricle: macular organization and hair bundle heights. J Neurophysiol 99:718-733. CrossRef Medline
45. Lim R, Kindig AE, Donne SW, Callister RJ, Brichta AM (2011) Potassium accumulation between type I hair cells and calyx terminals in mouse crista. Exp Brain Res 210:607-621. CrossRef Medline
46. Lysakowski A, Goldberg JM (1997) Regional variations in the cellular and synaptic architecture of the chinchilla cristae. J Comp Neurol 389:419-443. CrossRef Medline
47. Lysakowski A, Minor LB, Fernández C, Goldberg JM (1995) Physiological identification of morphological distinct afferent classes innervating the cristae ampullares of the squirrel monkey. J Neurophysiol 73:1270-1281. Medline
48. Lysakowski A, Gaboyard-Niay S, Calin-Jageman I, Chatlani S, Price SD, Eatock RA (2011) Molecular microdomains in a sensory terminal, the vestibular calyx ending. J Neurosci 31:10101-10114. CrossRef Medline
49. Marcotti W, Johnson SL, Rusch A, Kros CJ (2003) Sodium and calcium currents shape action potentials in immature mouse inner hair cells. J Physiol 552:743-761. CrossRef Medline
50. McCue MP, Guinan JJ Jr (1994) Acoustically responsive fibers in the vestibular nerve of the cat. J Neurosci 14:6058-6070. Medline
51. Meredith FL, Benke TA, Rennie KJ (2012) Hyperpolarization-activated current (Ih) in vestibular calyx terminals: Characterization and role in shaping postsynaptic events. J Assoc Res Otolaryngol 13:745-758. CrossRef Medline
52. Ramachandran R, Lisberger SG (2006) Transformation of vestibular signals into motor commands in the vestibuloocular reflex pathways of monkeys. J Neurophysiol 96:1061-1074. CrossRef Medline
53. Rennie KJ, Streeter MA (2006) Voltage-dependent currents in isolated vestibular afferent calyx terminals. J Neurophysiol 95:26-32. Medline
54. Ricci AJ, Kennedy HJ, Crawford AC, Fettiplace R (2005) The transduction channel filter in auditory hair cells. J Neurosci 25:7831-7839. CrossRef Medline
55. Rothman JS, Manis PB (2003) The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. J Neurophysiol 89:3097-3113. CrossRef Medline
56. Rusch A, Eatock RA (1996) A delayed rectifier conductance in type I hair cells of the mouse utricle. J Neurophysiol 76:995-1004. Medline
57. Rusch A, Eatock RA (1997) Sodium currents in hair cells of the mouse utricle. In: Diversity in auditory mechanics (Lewis ER, Long GR, Lyon RF, Steele CR, Narins PM, Hecht-Poinar E, eds), pp 549-555. Singapore: World Scientific.
58. Rusch A, Lysakowski A, Eatock RA (1998) Postnatal development of type I and type II hair cells in the mouse utricle: acquisition of voltage-gated conductances and differentiated morphology. J Neurosci 18:7487-7501. Medline
59. Rutherford MA, Roberts WM (2006) Frequency selectivity of synaptic exocytosis in frog saccular hair cells. Proc Natl Acad Sci U S A 103:2898-2903. CrossRef Medline
60. Sadeghi SG, Chacron MJ, Taylor MC, Cullen KE (2007) Neural variability, detection thresholds, and information transmission in the vestibular system. J Neurosci 27:771-781. CrossRef Medline
61. Schessel DA, Ginzberg R, Highstein SM (1991) Morphophysiology of synaptic transmission between type I hair cells and vestibular primary afferents. An intracellular study employing horseradish peroxidase in the lizard, Calotes versicolor. Brain Res 544:1-16. Medline
62. Schnee ME, Lawton DM, Furness DN, Benke TA, Ricci AJ (2005) Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 47:243-254. CrossRef Medline
63. Schweizer FE, Savin D, Luu C, Sultemeier DR, Hoffman LF (2009) Distribution of high-conductance calcium-activated potassium channels in rat vestibular epithelia. J Comp Neurol 517:134-145. CrossRef Medline
64. Sterkers O, Ferrary E, Amiel C (1988) Production of inner ear fluids. Physiological Rev 68:1083-1128. Medline
65. Vollrath MA, Eatock RA (2003) Time course and extent of mechanotransducer adaptation in mouse utricular hair cells: comparison with frog saccular hair cells. J Neurophysiol 90:2676-2689. CrossRef Medline
66. Wang LY, Fedchyshyn MJ, Yang YM (2009) Action potential evoked transmitter release in central synapses: insights from the developing calyx of Held. Mol Brain 2:36. CrossRef Medline
67. Weiss TF (1984) Relation of receptor potentials of cochlear hair cells to spike discharges of cochlear neurons. Annu Rev Physiol 46:247-259. CrossRef Medline
68. Weisz C, Glowatzki E, Fuchs P (2009) The postsynaptic function of type II cochlear afferents. Nature 461:1126-1129. CrossRef Medline
69. Wittig JH Jr, Parsons TD (2008) Synaptic ribbon enables temporal precision of hair cell afferent synapse by increasing the number of readily releasable vesicles: a modeling study. J Neurophysiol 100:1724-1739. CrossRef Medline
70. Wooltorton JR, Gaboyard S, Hurley KM, Price SD, Garcia JL, Zhong M, Lysakowski A, Eatock RA (2007) Developmental changes in two voltage-dependent sodium currents in utricular hair cells. J Neurophysiol 97:1684-1704. Medline
71. Yamashita M, Ohmori H (1990) Synaptic responses to mechanical stimulation in calyceal and bouton type vestibular afferents studied in an isolated preparation of semicircular canal ampullae of chicken. Exp Brain Res 80:475-488. Medline
72. Yamashita M, Ohmori H (1991) Synaptic bodies and vesicles in the calyx type synapse of chicken semicircular canal ampullae. Neurosci Lett 129: 43-46. CrossRef Medline